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Articles

Maternal Perception of the Onset of Lactation Is a Valid, Public Health Indicator of Lactogenesis Stage II¹

Department of Nutritional Science, University of Connecticut, Storrs, CT 06269

²To whom correspondence should be addressed. E-mail: djc{at}discovernet.net

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

 
Test weighing is the "gold standard" for documenting lactogenesis stage II. However, this method is impractical for use in population studies. Maternal perception of the timing of the onset of lactation may be a useful proxy for lactogenesis stage II. This study seeks to validate maternal perception of the onset of lactation as a marker of lactogenesis stage II. Women (n = 60) were recruited after cesarean delivery. Beginning at 24 h postpartum (pp), the onset of lactation was assessed 3 times daily by both test weighing and maternal perception. Delayed onset of lactation was defined as follows: 1) milk transfer < 9.2 g/feeding at 60 h pp and 2) maternal perception 72 h pp. Misclassification analyses were conducted. Multivariate logistic regression, bivariate analyses and Cox survival analyses were used to evaluate the determinants and consequences of delayed onset of lactation, using both definitions. The sensitivity and specificity of delayed maternal perception as an indicator of delayed lactogenesis were 71.4 and 79.3%, respectively. Four risk factors for low milk transfer were significant (P < 0.05) or nearly significant (P 0.08) predictors of delayed perception of the onset of lactation. The effects of low milk transfer and delayed maternal perception on breast-feeding duration were similarly modified by intended breast-feeding duration. The magnitude and directionality of the ß coefficients for the milk transfer and perception variables were consistent. On the basis of these results, we conclude that maternal perception of the onset of lactation is a valid public health indicator of lactogenesis stage II.

KEY WORDS: • breast-feeding • lactogenesis stage II • test weighing • cesarean delivery • lactation

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

 
The measurement of milk transfer by test weighing is considered to be the "gold standard" for documenting lactogenesis stage II (i.e., the initiation of copious secretion of breast milk after delivery) (Daly and Hartmann 1995 ). Unfortunately, test weighing is costly, invasive and impractical to use in population studies. Biochemical indices of lactogenesis stage II have been developed (Arthur et al. 1989 , Kulski and Hartmann 1981 , Neubauer et al. 1993 , Neville 1995 ). However, these methods require milk sampling and laboratory analyses, rendering them impractical for routine clinical assessment or use in large-scale studies. Reliable, inexpensive and noninvasive alternatives to test weighing or biochemical analyses have not been developed. From a public health perspective, maternal perception of the timing of the onset of lactation may be a useful proxy for lactogenesis stage II because it describes when women actually feel their breast milk "came in." The symptoms commonly reported to confirm the onset of lactation (Chapman and Pérez-Escamilla 1999b ) (i.e., breast fullness, engorgement, leaking) are consistent with the physiology of lactogenesis stage II and may indicate a milk supply that is more than adequate (Chen et al. 1998 , Hartmann et al. 1996 ). Maternal perception is admittedly subjective, however, and has not been established as a valid marker of lactogenesis stage II.

Few researchers have investigated the onset of lactation by collecting data on both maternal perception and milk transfer. Arthur et al. (1989) studied indicators of lactogenesis in Australian women after vaginal delivery and observed significant increases in milk transfer between 24 and 48 h postpartum (pp), signaling lactogenesis stage II. These changes in milk transfer coincided with increases in breast milk lactose and citrate concentrations. The biochemical and milk transfer indicators of lactogenesis preceded maternal report that milk had "come in" by at least 11 h. Because maternal perception of the onset of lactation occurred later than the phenomenon was documented by test weighing, Arthur and colleagues concluded that maternal perception of "milk arrival" is not a viable marker of lactogenesis stage II.

We postulate, however, that although women perceive the onset of lactation later than its occurrence is indicated by biochemical or test weighing analyses, this may be a systematic phenomenon. Thus, maternal perception may be a useful indicator of lactogenesis stage II. Maternal perception cannot be used with "to the minute" accuracy, but it can be used to differentiate women who perceive the onset of lactation to be early (i.e., <72 h pp) vs. late (i.e., 72 h pp). We hypothesized that perception of the onset of lactation (early vs. late) is likely to correspond with the level of milk transfer (high vs. low). Thus, maternal perception may be used as a valid indicator to examine the determinants and infant feeding consequences of the timing of lactogenesis.

The objective of this study is to substantiate the use of maternal perception of the onset of lactation as a marker of lactogenesis stage II. Specifically, this study compares the determinants and consequences of delayed onset of lactation after cesarean delivery, as measured by both test weighing and maternal perception.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

 
Subjects

Healthy breast-feeding women (n = 60) who gave birth by cesarean delivery at Hartford Hospital, Hartford, CT were recruited to participate in this study between June 1997 and November 1998 as described previously (Chapman 1999 ). Subjects were primarily recruited 8 to 24 h after delivery of a healthy singleton; however, three were recruited prenatally. Final analyses include 57 women because two subjects were dropped due to ineffective infant suckling and one was dropped due to poor compliance with study protocol. Baseline data were collected on nonparticipants. Between-group baseline characteristics (participants vs. nonparticipants) were compared using Student’s t test and ² analyses. Subjects were primarily Caucasian, married and 31 y old, with some college education. Overall, subjects had baseline characteristics similar to the 111 women who declined to participate in the study (Table 1 ). The only significant difference between participants and nonparticipants was that participants intended to breast-feed for 1.5 mo longer than those who declined. This study was approved by the Institutional Review Boards at the University of Connecticut and Hartford Hospital, Hartford, CT.

Data used in this methodologic evaluation of the perceived onset of lactation were obtained from a randomized clinical trial, designed to evaluate the effect of breast pumping on the onset of lactation (Chapman 1999 ). In that study, 57 subjects were randomly assigned to either a breast pumping group or a control group. Beginning at 24 h pp, subjects in the pumping group used a double electric breast pump (Lactina Select, Double Pumping Kit, Medela, McHenry, IL) for 10–15 min, three times daily after breast-feeding. Using this same time frame, those in the control group held the breast shields of the electric pump to their breasts, but did not turn on the pump. The onset of lactation was assessed three times daily by test weighing and maternal perception. In this analysis, the determinants and consequences of delayed onset of lactation, as defined by these two indicators, are evaluated.

Test weighing

    Procedure. Beginning at 24 h pp, infants were weighed before and after three breast-feeding sessions per day to determine milk transfer/feeding. The times of these feedings were 0842 ± 0102, 1321 ± 0155 and 1846 ± 0102 h. Test weights were obtained in triplicate by research staff using an electronic integrated scale fitted with an infant seat and a recording printer (model BP34; Sartorius, Goettingen, Germany). The manufacturer’s stated accuracy for the scale is ±0.05 g. Each printed weight was the average of 20 consecutive measurements. Women were not provided with the results of the test weighing. Insensible water loss was measured over one 15-min period. Test weighing continued until the onset of lactation was verified by both test weights (i.e., sharp increase in milk transfer curve, typically associated with milk transfer 15 g/feeding) and maternal perception of the onset of lactation.

If subjects were discharged from the hospital before the onset of lactation, test weights were obtained by the subject at home, as described previously (Dewey et al. 1991 , Ferris et al. 1993 , Neville et al. 1988 , Neubauer et al. 1993 ). Research staff delivered the same model of electronic balance to the subject’s home on the date of discharge. The subject and interested family members received verbal and written instructions on test weighing procedures and were required to demonstrate their ability to use the balance before collecting data. Subjects were requested to weigh their newborns before and after three feeding sessions per day until advised to stop by research staff. Researchers were available by pager and remained in telephone contact with the subjects to ensure compliance with the test weighing protocol.

    Milk transfer curves. Milk transfer data were adjusted for insensible water loss, which was measured individually. For the 12 infants with missing data for insensible water loss, the mean [1.29 g/(kg · h)] was used. Milk transfer was then plotted over time to generate individual milk transfer curves. These curves were fitted to the quadratic equation to generate predicted milk transfer curves for each mother-infant pair. The coefficients of each individual predictive curve were then used to predict milk transfer for 24, 30, 36, 48, 60 and 72 h pp.

Maternal perception

Assessment of maternal perception of the onset of lactation began at 24 h pp. To evaluate the clinical symptoms of lactogenesis, subjects were interviewed regarding breast symptoms (i.e., breast fullness, swelling, leakage) three times daily, immediately after the test weights were completed. Subjects were then asked "Has your milk come in yet?" If the response was positive, the subject was then asked, "When did your milk come in?"; the response to this question was recorded to the nearest hour. Subjects routinely reported breast symptom changes before reporting that the onset of lactation had occurred. No attempt was made to coach subjects on the clinical indicators of lactogenesis. Subjects who were discharged before the onset of lactation (n = 11) were contacted at least daily by research staff to determine the timing of maternal perception of the onset of lactation.

Follow-up data collection

Follow-up telephone interviews were conducted to assess the relationship between the timing of the onset of lactation and breast-feeding duration. Researchers contacted subjects 6 mo pp to determine the duration of both exclusive and any breast-feeding. If subjects were still breast-feeding, additional follow-up calls were made at 4-mo intervals. Data analysis was conducted 6 mo after the last subject was enrolled into the study. At the time of data analysis, 30% of subjects were still breast-feeding, and the average breast-feeding duration was 6.3 ± 4.8 mo.

Model specification: determinants of delayed onset of lactation

Multivariate logistic regression analyses were used to identify the independent effects of the determinants of delayed onset of lactation. All statistical analyses were conducted using SPSS for Windows, Version 8.0 (Norusis 1992 ), and were interpreted using P 0.05 (two-tailed) as level of significance.

    Dependent variables. Two multivariate logistic regression models were developed, differing only in the definition of the dependent variable, i.e., the timing of the onset of lactation. In the "maternal perception model," the perceived timing of the onset of lactation was characterized as early or late (<72 h pp vs. 72 h pp), as described previously (Chapman and Pérez-Escamilla 1999b ).

For the "milk transfer model," predicted milk transfer at 60 h pp was defined as high or low, using the sample mean (n = 57) as a cut-off value (9.2 g/feeding vs. <9.2 g/feeding), as described previously (Chapman 1999 ). The time frame of 60 h pp was chosen because 55.4% of subjects had perceived milk arrival by 72 h pp, and test weighing had frequently been discontinued. Rather than establishing a milk transfer definition based on predicted curves extending beyond the limits of our raw data (i.e., at 72 h pp), we chose to use 60 h pp, the point at which 98% of subjects had milk transfer data. The predicted milk transfer curves provided a useful estimate of actual milk transfer values. The overall correlation coefficient for the actual vs. predicted curves was 0.84. The average predicted value for milk transfer at 60 h pp was 94% of the corresponding value derived by averaging raw data. Because of these close correlations with actual milk transfer data, using predictive milk transfer curves was deemed more objective than determining the inflection point for each individual curve.

    Independent variables. The multivariate logistic regression models included 10 main effects and two two-way interactions.

Maternal factors. Maternal obesity has been associated with delayed perception of the onset of lactation (Chapman and Pérez-Escamilla 1999b ). Because of fluid retention in the immediate postpartum period, the assessment of maternal obesity at the time of delivery is challenging. Our approach was to assess three indicators of maternal obesity. Women were classified as obese if at least two of these three indicators were positive: body mass index at 72 h pp 30 kg/m², subscapular skinfold thickness at 72 h pp more than the 85th percentile of our study data (i.e., >33.7 mm) and heavy/obese body build on d 1 pp (vs. slim/average body build). Tricep skinfold measurements were not used because previous research demonstrated that these measurements are unreliable markers of body fat during lactation (Brewer et al. 1989 ).

Ethnicity was categorized as African American vs. all other ethnic groups on the basis of the previous identification of non-African American ethnicity as a risk factor for delayed onset of lactation (Chapman and Pérez-Escamilla 1999b ). Parity was categorized as primiparous vs. multiparous and was included in the model due to documented differences in milk transfer (Chapman 1999 ) and perception of the onset of lactation among primiparae vs. multiparae (Chapman and Pérez-Escamilla 1999b ). Because of the potential for maternal age to affect the timing of the onset of lactation, age was entered as a continuous variable.

Early breast-feeding factors. Previous research suggests that early breast-feeding initiation (Sozmen 1992 ) and frequent breast-feeding (Salariya et al. 1978 , Sozmen 1992 ) may hasten the onset of lactation. The time of breast-feeding initiation was categorized as early vs. late, using the median as a cut-off value (i.e., 105 vs. >105 min pp). Breast-feeding frequency during the first 24 h pp was classified as high (7 feedings) vs. low (<7 feedings) on the basis of the mean. These data were derived by maternal recall, obtained between 24 and 36 h pp. For the seven subjects with missing data, breast-feeding frequency during the first 24 h was obtained from the medical record. Predicted milk transfer at 30 h pp was expressed as a continuous variable.

Infant/delivery factors. Birth weight < 3.5 kg has been identified as a risk factor for delayed onset of lactation (Chapman and Pérez-Escamilla 1999b ). Thus birth weight was categorized as below or above the mean (<3.5 kg vs. 3.5 kg). Due to the previous identification of unscheduled cesarean delivery as a risk factor for delayed onset of lactation (Chapman and Pérez-Escamilla 1999b ), delivery type was expressed as scheduled vs. unscheduled.

Study group. Because of the potential for group assignment to affect the timing of the onset of lactation, study group was classified as pumping vs. control.

Interaction terms. Parity · study group was included in the model to test the hypothesis that the effect of breast pumping on the onset of lactation was modified by parity. To evaluate our post-hoc hypothesis that the onset of lactation occurs later in obese women as a result of less frequent nursing, we included the breast-feeding frequency · maternal obesity interaction term.

Model specification: determinants of the duration of any breast-feeding

Multivariate survival analyses (Cox model) were used to identify the determinants of the duration of any breast-feeding, after controlling for potential confounders.

    Dependent variable. The duration of any breast-feeding was assessed during follow-up telephone interviews made to subjects between 2 and 19 mo pp. One subject was lost to follow-up; thus the breast-feeding duration models include 56 subjects. In total, four models were evaluated. For women who were still breast-feeding when the last contact was made, the duration of any breast-feeding was identified as right censored in the Cox regression model.

    Independent variables. Series 1. The first series included two models, each consisting of 10 main effects. Each model included one indicator of lactogenesis stage II, based on either milk transfer or maternal perception.

Maternal factors. Maternal obesity (Hilson et al. 1997 , Rutishauser and Carlin 1992 ), education level (Ford and Labbok 1990 , Michaelsen et al. 1994 , Quarles et al. 1994 ), parity (Chapman and Pérez-Escamilla 1999a , Ford and Labbok 1990 ), employment status (Chapman and Pérez-Escamilla 1999a , Pérez-Escamilla et al. 1993 ), age (Ford and Labbok 1990 , Michaelsen et al. 1994 , Samuels et al. 1985 ) and group assignment (Chapman 1999 ), have all been shown to affect the duration of breast-feeding. Maternal obesity, education level and parity were expressed categorically, as described in the "determinants of delayed onset of lactation" model specifications. Maternal employment status at the time of the last follow-up call was entered as a three-category (full-time, part-time, not employed outside of the home) dummy variable. Maternal age was expressed as a continuous variable.

Early infant feeding practices. Early infant feeding practices, including the frequency of breast-feeding in the first 24 h after delivery (Salariya et al. 1978 , Sozmen 1992 ), the timing of the onset of lactation (Chapman and Pérez-Escamilla 1999a , Ferris et al. 1987 , McCabe 1982 , Pérez-Escamilla et al. 1993 and 1996 , Segura-Millan et al. 1994 ) and the use of prelacteal feedings (Pérez-Escamilla et al. 1996 , Samuels et al. 1985 ), can affect breast-feeding duration.

Breast-feeding frequency during the first 24 h pp, milk transfer at 60 h pp and maternal perception of the onset of lactation at 72 h were categorized as described in the "determinants of delayed onset of lactation" model. (Only one term describing the timing of the onset of lactation was included per model.) Data on the use of prelacteal feedings (yes/no) were obtained from daily interviews and confirmed by medical record review.

Intended breast-feeding duration. Women planning to breast-feed for <6 mo are at risk for early breast-feeding termination (Chapman and Pérez-Escamilla 1999a , Loughlin et al. 1985 ). On d 1 pp, subjects were asked for how long they planned to breast-feed, using an open-ended question. Intended breast-feeding duration was entered as a dichotomous variable (<6 mo vs. 6 mo).

    Series 2. Intended breast-feeding duration modifies the association between the onset of lactation and actual breast-feeding duration (Chapman and Pérez-Escamilla 1999a ). In the second series of models, we attempted to evaluate this relationship. The two models in series 2 each contained nine main effects. Eight of the main effects were identical to those of series 1 (maternal obesity, education level, parity, group assignment, employment status, age, breast-feeding frequency in first 24 h pp and use of prelacteal feedings). In addition, a new three-term variable was developed to combine intended breast-feeding duration and the onset of lactation. For this variable, the subgroups planning to breast-feed <6 mo were combined. This was done for the following reasons: 1) the strong similarities in breast-feeding duration and small sample size (n = 7) of these subgroups in the current study; and 2) previous research indicating that the onset of lactation does not affect breast-feeding duration among women planning to breast-feed for <6 mo (Chapman and Pérez-Escamilla 1999a ). Thus, the milk transfer and maternal perception model each contain one three-term variable, based on their respective definitions of delayed onset of lactation (i.e., intended breast-feeding duration < 6 mo vs. early onset of lactation and planning to breast-feed 6 mo vs. late onset of lactation and planning to breast-feed 6 mo).

Model specification: determinants of the duration of exclusive breast-feeding

    Dependent variable. The duration of exclusive breast-feeding was assessed through follow-up telephone interviews. At the time of final data analyses, all subjects had discontinued exclusive breast-feeding. The duration of exclusive breast-feeding ranged from 0.1 to 6.0 mo, with a mean of 3.0 ± 1.7 mo.

    Independent variables. The determinants of the duration of exclusive breast-feeding in the United States have not been well characterized. Therefore, the independent variables used to model the determinants of the duration of any breast-feeding were also utilized to model the duration of exclusive breast-feeding in our population. As in the previous series of models, a total of four multivariate survival analyses models were evaluated.

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

 
The sensitivity and specificity of delayed maternal perception of the onset of lactation as an indicator of delayed lactogenesis stage II were 71.4% (20/28) and 79.4% (23/29), respectively. The positive and negative predictive values were 76.9 and 74.2%, respectively. Within the pumping group, the sensitivity and specificity of delayed perception were 78.6% (11/14) and 71.4% (10/14), respectively. For subjects in the control group, the sensitivity and specificity of maternal perception were 64.4% (9/14) and 86.7% (13/15), respectively.

Determinants of delayed onset of lactation.

Five variables were identified as significant risk factors for delayed onset of lactation (Table 2 ). Two of these terms (breast-feeding initiation later than 105 min pp and parity · study group interaction) were significant in both the milk transfer and maternal perception models. Two terms (lower milk transfer at 30 h and the obesity · breast-feeding frequency interaction during the first 24 h pp) were significant in the milk transfer model and approached significance in the maternal perception model. Unscheduled cesarean delivery was a significant risk factor unique to the maternal perception model.

View larger version (44K): [in this window] [in a new window]   Figure 1. Effect of pumping on the probability of delayed onset of lactation modified by parity [delayed onset of lactation defined as low milk transfer (A) and delayed maternal perception (B)].

View larger version (51K): [in this window] [in a new window]   Figure 2. Effect of breast-feeding frequency during the first 24 h postpartum on the probability of delayed onset of lactation modified by maternal obesity [delayed onset of lactation defined as low milk transfer (A) and as delayed perception (B)].

	Consequences of delayed onset of lactation

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

As main effects, neither low milk transfer nor delayed perception of the onset of lactation were identified as risk factors for discontinuing breast-feeding. Planning to breast-feed for <6 mo (P < 0.05) and full-time employment (P < 0.05) were identified as significant risk factors for early termination of breast-feeding in both series 1 models. Breast-feeding < 7 times in the first 24 h pp significantly increased the risk of discontinuing breast-feeding in the milk transfer model (P < 0.05) and approached significance (P < 0.08) in the perception model. In both models, maternal obesity tended to have a positive effect on the duration of any breast-feeding (P = 0.06–0.10).

The three-term variables used in series 2 (combining onset of lactation with intended breast-feeding duration) were first evaluated in a bivariate model. The unadjusted breast-feeding duration values associated with the three-term variables displayed a significant dose-response relationship. Breast-feeding duration was longest for those planning to breast-feed for at least 6 mo and experiencing an early onset of lactation. It decreased for their counterparts experiencing a delayed onset of lactation, and was shortest for those planning to breast-feed for <6 mo. This dose-response effect was evident when the onset of lactation was defined by milk transfer (P < 0.0001) and by maternal perception (P < 0.0001).

In the series 2 multivariate model, three terms were identified as significant risk factors for early termination of breast-feeding in both models (low breast-feeding frequency on day 1 pp, full time employment and planning to breast-feed for <6 mo) (Table 3 ). Maternal obesity was associated with significantly longer breast-feeding duration in the milk transfer model and approached significance in the maternal perception model (P < 0.08). Among women planning to breast-feed for 6 mo, those with early perception of the onset of lactation breast-fed significantly longer than their counterparts with a delayed onset of lactation.

As main effects, neither definition of delayed onset of lactation was a significant risk factor for shorter duration of exclusive breast-feeding; however, their ß coefficients were nearly identical (0.41 for the milk transfer model, and 0.40 for the maternal perception model). Maternal education level < 16 y was identified as the only significant risk factor (P < 0.05) for early termination of exclusive breast-feeding in the series 1 maternal perception model, and this was the only term to approach significance in the milk transfer model (P = 0.10).

In the bivariate model, the three-term variable combining the timing of the onset of lactation with intended breast-feeding duration yielded a dose-response relationship for the duration of exclusive breast-feeding. As was observed for the duration of any breast-feeding, women experiencing early onset of lactation and intending to breast-feed for at least 6 mo had the longest duration of exclusive breast-feeding, followed by those with late onset of lactation and plans to breast-feed for at least 6 mo, and those intending to breast-feed for <6 mo, respectively. This relationship was significant in the milk transfer model (P = 0.02) and approached significance in the maternal perception model (P = 0.06).

In the series 2 multivariate model, the three-term variable approached significance in the milk transfer model (P = 0.13) (Table 4 ). Among women planning to breast-feed for at least 6 mo, those with higher milk transfer values at 60 h pp tended to breast-feed exclusively for longer than their counterparts with lower milk transfer values. The ß coefficients for the comparisons of early vs. late onset of lactation among women who intended to breast-feed for at least 6 mo were of similar magnitude and directionality (ß = 0.66 in the milk transfer model and 0.47 in the maternal perception model). Maternal education level < 16 y approached significance as a risk factor for early termination of exclusive breast-feeding in both models (P = 0.07).

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

Our findings coincide with previous studies assessing maternal perception of the onset of lactation, in combination with other indicators of lactogenesis. Using biochemical markers, Arthur et al. (1989) demonstrated delayed lactogenesis among diabetic vs. control subjects. This was supported by a nearly significant delay in maternal perception (P < 0.06) among the four diabetic women who perceived the onset of lactation. In a similar series of studies (Ferris et al. 1993 , Neubauer et al. 1993 ), maternal perception, breast milk intake on d 7 pp and biochemical markers of lactogenesis consistently indicated delayed lactogenesis among control subjects and those with insulin-dependent diabetes mellitus, compared with their reference group. Chen et al. (1998) evaluated four indicators of lactogenesis, including maternal perception of the onset of breast fullness. Although this term differs from our definition of maternal perception, maternal/fetal stress markers were associated with delays in both breast fullness and casein appearance. The timing of the onset of breast fullness was highly correlated with milk volume on d 5 pp and with casein appearance. Delayed lactogenesis was demonstrated among primiparae (vs. multiparae) by both delayed breast fullness and decreased milk volume on d 5. Chen and colleagues (1998) caution that maternal perception of breast fullness may not always be a useful indicator of lactogenesis, especially in situations in which decreased breast-feeding frequency may result in engorgement.

The determinants of delayed onset of lactation that we have identified either confirm previous findings or provide new insights. The identification of delayed breast-feeding initiation as a risk factor for delayed onset of lactation supports the findings of Sozmen (1992) and Salariya et al. (1978) . The consistently significant interaction between parity and study group demonstrates that breast pumping between 24 and 72 h after cesarean delivery delays the onset of lactation among primiparae and therefore should be avoided. As expected, low milk transfer at 30 h pp predicts low milk transfer at 60 h pp and tends to predict delayed maternal perception. The absence of a stimulatory effect of early, frequent breast-feeding in the first 24 h pp on the onset of lactation among obese women has not been described previously. This finding may explain in part why obese women perceive the onset of lactation later than slim or average women (Chapman and Pérez-Escamilla 1999b ) and are less successful initiating breast-feeding (Hilson et al. 1997 ). Possible explanations include decreased ability to perceive breast fullness or elevated levels of steroid hormones/leptin among obese women in the early post-partum period (Chapman and Pérez-Escamilla 1999b ). This area requires further investigation.

The identification of unscheduled cesarean delivery as a significant risk factor for delayed perception of the onset of lactation supports our previous findings (Chapman and Pérez-Escamilla 1999b ) and the conclusions of Chen et al. (1998) that delivery-related stress has a negative effect on the onset of lactation. The type of cesarean delivery (scheduled vs. unscheduled), however, did not significantly affect milk transfer. This delay in perception, despite similar milk transfer values, may be related to maternal exhaustion or the use of anesthesia. In this study, delivery type and anesthesia type (spinal vs. epidural) were collinear variables; thus the effect of these terms could not be disentangled.

The consequences of late onset of lactation on breast-feeding duration were similar, regardless of how the independent variable was defined. Our data replicate our previous finding (Chapman and Pérez-Escamilla 1999a ) that among women planning to breast-feed for at least 6 mo, those with delayed perception of the onset of lactation are more likely to discontinue breast-feeding sooner than their counterparts who perceived it earlier. In the bivariate analyses, the duration of any breast-feeding decreased significantly in a dose-response fashion when comparing subgroups of the intended breast-feeding duration/onset of lactation three-term variable. This significant bivariate dose-response relationship was replicated for the duration of exclusive breast-feeding when milk transfer was a component of the three-term variable, and approached significance with maternal perception in the three-term variable. With a larger sample size, it is likely that the latter would have been significant.

Five main effects were consistently significant or nearly significant risk factors for short breast-feeding duration. Our data support previous research documenting the negative effects of the following: 1) planning to breast-feed for <6 mo (Loughlin et al. 1985 , McCabe 1982 , Pérez-Escamilla et al. 1993 and 1997 , Quarles et al. 1994 ); 2) low breast-feeding frequency in the early pp period (Salariya et al. 1978 ); 3) full-time employment (Samuels et al. 1985 ); and 4) the interaction between the onset of lactation and intended breast-feeding duration (Chapman and Pérez-Escamilla 1999a ) on the duration of any breast-feeding. Our finding that obese women were more likely to breast-feed longer (P = 0.05–0.10) than their nonobese counterparts is in contrast to previous research (Hilson et al. 1997 , Rasmussen 1998 , Rutishauser and Carlin 1992 ). This association persisted, even after removal of the milk transfer and maternal perception variables from the model. Our findings suggest that maternal obesity may not necessarily interfere with breast-feeding success, if in-depth breast-feeding support is provided through the onset of lactation.

Because our data were obtained from women who gave birth via cesarean delivery and were enrolled in a breast pumping study, the external validity of our findings may be limited. Women undergoing cesarean delivery may not be representative of the general population. We have shown previously that women delivering by unscheduled cesarean delivery (43% of the subjects in this study) are more likely to have a delayed perception of the onset of lactation than those delivering vaginally with a short stage II labor (Chapman and Pérez-Escamilla 1999b ). Subjects in the pumping group visualized the residual milk after a feeding, potentially becoming more aware of milk production levels than the average postpartum woman. This could have exaggerated the predictive ability of maternal perception. This does not appear to be the case because the sensitivity of maternal perception as an indicator of delayed lactogenesis was better among the pumping subjects, whereas the specificity of maternal perception was better among controls.

In conclusion, our findings strongly suggest that maternal perception of the onset of lactation is a useful public health indicator of lactogenesis stage II. This conclusion is based on the misclassification analyses and the similarities in the determinants and consequences of low milk transfer and delayed maternal perception of the onset of lactation in our population. When posing questions on the determinants and consequences of delayed lactogenesis, essentially the same conclusions would be reached regardless of the definition of lactogenesis II.

Our findings suggest that it is worthwhile for clinicians to evaluate maternal perception of the onset of lactation, given its ease of use and high degree of correlation with the expensive and invasive standard of test weighing. Women who are attempting to breast-feed do not routinely have access to biochemical markers of lactogenesis. Thus, they are likely to base their infant feeding decisions on their perception of the adequacy of their breast milk supply. By asking women when they perceived the onset of lactation, health care providers can identify women at risk for poor breast-feeding outcomes in a cost-effective manner. Women with delayed perception of the onset of lactation may benefit from additional breast-feeding support because women planning to breast-feed for at least 6 mo often do not reach their goal if the onset of lactation is perceived to be late (Chapman and Pérez-Escamilla 1999a ).

Our conclusions should not be interpreted to suggest that maternal perception should replace milk transfer in all future research studies. On the contrary, we support the use of the most accurate methods for determining the timing of the onset of lactation. However, in large-scale studies, in which test weighing or biochemical analyses are prohibitively expensive, maternal perception appears to be a useful indicator of lactogenesis. Future studies are required in different cultures and settings to conclusively validate maternal perception of the onset of lactation as a marker of lactogenesis stage II.

	ACKNOWLEDGMENTS

 
The authors gratefully acknowledge their appreciation to all of the families who generously participated in this study. We are grateful to Aleja Rosario, Jocelyn Cruz, Paula McKernan, Ann-Marie Nocton and Melissa Wills for their expert assistance with data collection. We thank the staff of Hartford Hospital Women’s Health Services for their support of this project.

	FOOTNOTES

 
¹ Funded by the University of Connecticut Research Foundation, the Connecticut Family Nutrition Program for Infants, Toddlers and Children and Hartford Hospital Research Administration. We are grateful to Medela, Incorporated for "in kind" support. This article is scientific contribution number 1978, Storrs Agricultural Experiment Station, University of Connecticut, Storrs, CT.

³ To whom reprint requests should be addressed. E-mail: rperez{at}canr.cag.uconn.edu

Manuscript received June 6, 2000. Initial review completed July 26, 2000. Revision accepted September 6, 2000.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS Consequences of delayed onset... DISCUSSION REFERENCES

 

1. Arthur P., Smith M., Hartmann P. Milk lactose, citrate and glucose as markers of lactogenesis in normal and diabetic women. J. Pediatr. Gastroenterol. Nutr. 1989;90:488-496

2. Brewer M., Bates M., Vannoy L. Postpartum changes in maternal weight and body fat depots in lactating vs nonlactating women. Am. J. Clin. Nutr. 1989;49:259-265[Abstract/Free Full Text]

3. Chapman D. The Impact of Breast Pumping on the Onset of Lactogenesis Stage II following Cesarean Delivery: A Randomized Clinical Trial 1999 University of Connecticut Storrs, CT Doctoral thesis

4. Chapman D., Pérez-Escamilla R. Does delayed perception of the onset of lactation shorten breastfeeding duration?. J. Hum. Lact. 1999a;15:107-111[Abstract/Free Full Text]

5. Chapman D., Pérez-Escamilla R. Identification of risk factors for delayed onset of lactation. J. Am. Diet. Assoc. 1999b;99:450-454[Medline]

6. Chen D., Nommsen-Rivers L., Dewey K., Lönnerdal B. Stress during labor and delivery and early lactation performance. Am. J. Clin. Nutr. 1998;68:335-344[Abstract]

7. Daly S., Hartmann P. Infant demand and milk supply: Part 2: the short-term control of milk synthesis in lactating women.. J. Hum. Lact. 1995;11:27-37[Abstract/Free Full Text]

8. Dewey K., Heinig M., Nommsen L., Lönnerdal B. Adequacy of energy intake among breast-fed infants in the DARLING study: relationships to growth velocity, morbidity, and activity levels. J. Pediatr. 1991;119:538-547[Medline]

9. Ferris A. M., McCabe L. T., Allen L. H., Pelto G. H. Biological and sociocultural determinants of successful lactation among women in eastern Connecticut. J. Am. Diet. Assoc. 1987;87:316-321[Medline]

10. Ferris A., Neubauer S., Bendel R., Green K., Ingardia C., Reece E. Perinatal lactation protocol and outcome in mothers with and without insulin-dependent diabetes mellitus. Am. J. Clin. Nutr. 1993;58:43-48[Abstract/Free Full Text]

11. Ford K., Labbok M. Who is breast-feeding?: Implications of associated social and biomedical variables for research on the consequences of method of infant feeding. Am. J. Clin. Nutr. 1990;52:451-456[Abstract/Free Full Text]

12. Hartmann P., Owens R., Cox D., Kent J. Breast development and control of milk synthesis. Food Nutr. Bull. 1996;17:292-304

13. Hilson J., Rasmussen K., Kjolhede C. Maternal obesity and breast-feeding success in a rural population of white women. Am. J. Clin. Nutr. 1997;66:1371-1378[Abstract/Free Full Text]

14. Kulski J., Hartmann P. Changes in human milk composition during the initiation of lactation. Aust. J. Exp. Biol. Med. Sci. 1981;59:101-114[Medline]

15. Loughlin H., Clapp-Channing N., Gehlbach S., Pollard J., McCutchen T. Early termination of breast-feeding: identifying those at risk. Pediatrics 1985;75:508-513[Abstract/Free Full Text]

16. McCabe T. The Assessment of Factors That Affect the Duration of Lactation of Women Residing in Eastern Connecticut: A Predictive Model 1982 University of Connecticut Storrs, CT. Doctoral thesis

17. Michaelsen K., Larsen P., Thomsen B., Samuelson G. The Copenhagen cohort study on infant nutrition and growth: duration of breastfeeding and influencing factors. Acta Paediatr 1994;83:565-571[Medline]

18. Neubauer S., Ferris A., Chase C., Fanelli J., Thompson C., Lammi-Keefe C., Clark R., Jensen R., Bendel R., Green K. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am. J. Clin. Nutr. 1993;58:54-60[Abstract/Free Full Text]

19. Neville M. C. Determinants of milk volume and composition—lactogenesis in women: a cascade of events revealed by milk composition. Jensen R. G. eds. Handbook of Milk Composition 1995:87-98 Academic Press Boston, MA.

20. Neville M., Keller R., Seacat J., Lutes V., Neifert M., Casey C., Allen J., Archer P. Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactation. Am. J. Clin. Nutr. 1988;48:1375-1386[Abstract/Free Full Text]

21. Norusis, M. (1992) SPSS for Windows. Chicago, IL

22. Pérez-Escamilla R., Lutter C., Wickham C., Phillips M., Trevino-Siller S., Sanghvi T. Identification of risk factors for short breastfeeding duration in Mexico City through survival analysis. Ecol. Food Nutr. 1997;36:43-64

23. Pérez-Escamilla R., Segura-Millan S., Canahuati J., Allen H. Prelacteal feeds are negatively associated with breast-feeding outcomes in Honduras. J. Nutr. 1996;126:2765-2773

24. Pérez-Escamilla R., Segura-Millan S., Pollitt E., Dewey K. Determinants of lactation performance across time in an urban population from Mexico. Soc. Sci. Med. 1993;37:1069-1078

25. Quarles A., Williams P., Hoyle D., Brimeyer M., Williams A. Mothers’ intention, age, education and the duration and management of breastfeeding. Matern. Child Nurs. J. 1994;22:102-108[Medline]

26. Rasmussen K. Effects of under- and overnutrition on lactation in laboratory rats. J. Nutr. 1998;128:390S-393S

27. Rutishauser I., Carlin J. Body mass index and duration of breast feeding: a survival analysis during the first six months of life. J. Epidemiol. Community Health 1992;46:559-565[Abstract/Free Full Text]

28. Salariya E., Easton P., Cater J. Duration of breast-feeding after early initiation and frequent feeding. Lancet 1978;2:1141-1143[Medline]

29. Samuels S., Margen S., Schoen E. Incidence and duration of breast-feeding in a health maintenance organization population. Am. J. Clin. Nutr. 1985;44:504-510

30. Segura-Millan S., Dewey K., Pérez-Escamilla R. Factors associated with perceived insufficient milk in a low-income urban population in Mexico. J. Nutr. 1994;124:202-212

31. Sozmen M. Effects of early suckling of cesarean-born babies on lactation. Biol. Neonate 1992;62:67-68[Medline]

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